Abstract
Deleterious mutations inevitably emerge in any evolutionary process and are speculated to decisively influence the structure of the genome. Meiosis, which is thought to play a major role in handling mutations on the population level, recombines chromosomes via non-randomly distributed hot spots for meiotic recombination. In many genomes, various types of genetic elements are distributed in patterns that are currently not well understood. In particular, important (essential) genes are arranged in clusters, which often cannot be explained by a functional relationship of the involved genes. Here we show by computer simulation that essential gene (EG) clustering provides a fitness benefit in handling deleterious mutations in sexual populations with variable levels of inbreeding and outbreeding. We find that recessive lethal mutations enforce a selective pressure towards clustered genome architectures. Our simulations correctly predict (i) the evolution of non-random distributions of meiotic crossovers, (ii) the genome-wide anti-correlation of meiotic crossovers and EG clustering, (iii) the evolution of EG enrichment in pericentromeric regions and (iv) the associated absence of meiotic crossovers (cold centromeres). Our results furthermore predict optimal crossover rates for yeast chromosomes, which match the experimentally determined rates. Using a Saccharomyces cerevisiae conditional mutator strain, we show that haploid lethal phenotypes result predominantly from mutation of single loci and generally do not impair mating, which leads to an accumulation of mutational load following meiosis and mating. We hypothesize that purging of deleterious mutations in essential genes constitutes an important factor driving meiotic crossover. Therefore, the increased robustness of populations to deleterious mutations, which arises from clustered genome architectures, may provide a significant selective force shaping crossover distribution. Our analysis reveals a new aspect of the evolution of genome architectures that complements insights about molecular constraints, such as the interference of pericentromeric crossovers with chromosome segregation.
Highlights
Mating and meiosis are the masterpieces of an evolutionary invention thought to meet the challenges of changing environmental conditions that need to be solved by mutational inventions
Using an evolutionary computer simulation of diploid, unicellular sexual populations, we show that recessive lethal mutations can drive the evolution of chromosome architectures, in which essential genes become genetically linked into clusters
We find that several hallmarks of yeast chromosome crossing over during meiosis are consistent with natural selection imposed by recessive lethal mutations affecting essential genes
Summary
Mating and meiosis are the masterpieces of an evolutionary invention thought to meet the challenges of changing environmental conditions that need to be solved by mutational inventions. Among the many hypotheses that govern the various benefits of mating and meiosis [1], two main hypotheses stand out: enhanced purging of deleterious mutations [2] and the combination of beneficial alleles into one genome [3]. It remains a matter of discussion, which of these advantages constitutes the main reason for the evolution of sexual recombination and, its continuing prevalence in most eukaryotic life forms [4,5]. The accumulation of recessive deleterious mutations in yeast may not significantly decrease the fitness of the genotype or population growth rates, as long as the diploid nuclear condition is maintained [14]
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